Rapid deadenylation and Poly(A)-dependent translational repression mediated by the Caenorhabditis elegans tra-2 3' untranslated region in Xenopus embryos

Molecular and Cellular Biology

Volumn 20, Issue 6, 2000, Pages 2129-2137

  Thompson, Sunnie R ^a,c   Goodwin, Elizabeth B ^b   Wickens, Marvin ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYADENYLIC ACID;

3' UNTRANSLATED REGION; ADENYLATION; ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CELL FATE; CONSENSUS SEQUENCE; EMBRYO; EMBRYO PATTERN FORMATION; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; SEX DETERMINATION; SPERMATOGENESIS; TANDEM REPEAT; TRANSLATION REGULATION; XENOPUS;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HELMINTH PROTEINS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; OOCYTES; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; TANDEM REPEAT SEQUENCES; XENOPUS;

ANIMALIA; CAENORHABDITIS ELEGANS; EUKARYOTA; INVERTEBRATA;

EID: 0033993581     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.6.2129-2137.2000     Document Type: Article

References (64)

1. Audic, Y., F. Omilli, and H. B. Osborne. 1998. Embryo deadenylation element-dependent deadenylation is enhanced by a cis element containing AUU repeats. Mol. Cell. Biol. 18:6879-6884.
2. Ballantyne, S., A. Bilger, J. Astrom. A. Virtanen, and M. Wickens. 1995. Poly(A) polymerases in the nucleus and cytoplasm of frog oocytes: dynamic changes during oocyte maturation and early development. RNA 1:64-78.
3. Barker, D. D., C. Wang, J. Moore, L. K. Dickinson, and R. Lehmann. 1992. Pumilio is essential for function but not for distribution of the Drosophila abdominal determinant Nanos. Genes Dev. 6:2312-2326.
4. Beelman, C. A., and R. Parker. 1995. Degradation of mRNA in eukaryotes. Cell 81:179-183.
5. Bouvet, P., F. Omilli, Y. Arlot-Bonnemains, V. Legagneux, C. Roghi, T. Bassez, and H. B. Osborne. 1994. The deadenylation conferred by the 3′ untranslated region of a developmentally controlled mRNA in Xenopus embryos is switched to polyadenylation by deletion of a short sequence element. Mol. Cell. Biol. 14:1893-1900.
6. Chen, C. Y., and A. B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465-470.
7. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
8. Curtis, D., R. Lehmann, and P. D. Zamore. 1995. Translational regulation in development. Cell 81:171-178.
9. Dickson, K., A. Bilger, S. Ballantyne, and M. Wickens. 1999. Cleavage and polyadenylation specilicity factor in Xenopus laevis oocytes is a cytoplasmic factor involved in regulated polyadenylation. Mol. Cell. Biol. 19:5707-5717.
10. Doniach, T. 1986. Activity of the sex-determining gene tra-2 is modulated to allow spermatogenesis in the C. elegans hermaphrodite. Genetics 114:53-76.
11. Fan, X. C., and J. A. Steitz. 1998. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17:3448-3460.
12. Ford, L. P., J. Watson, J. Keene, and J. Wilusz. 1999. ELAV proteins stabilize deadenylated intermediates in a novel in vitro mRNA deadenylation/degradation system. Genes Dev. 13:188-201.
13. Fox, C. A., M. D. Sheets, E. Wahle, and M. Wickens. 1992. Polyadenylation of maternal mRNA during oocyte maturation: poly(A) addition in vitro requires a regulated RNA binding activity and a poly(A) polymerase. EMBO J. 11:5021-5032.
14. Fox, C. A., M. D. Sheets, and M. P. Wickens. 1989. Poly(A) addition during maturation of frog oocytes: distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU. Genes Dev. 3:2151-2162.
15. Fox, C. A., and M. Wickens. 1990. Poly(A) removal during oocyte maturation: a default reaction selectively prevented by specific sequences in the 3'UTR of certain maternal mRNAs. Genes Dev. 4:2287-2298.
16. Francis, R., M. K. Barton, J. Kimble, and T. Schedl. 1995. gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics 139:579-606.
17. Goodwin, E. B., P. G. Okkema, T. C. Evans, and J. Kimble. 1993. Translational regulation of tra-2 by its 3′ untranslated region controls sexual identity in C. elegans. Cell 75:329-339.
18. Gray, N. K., and M. Wickens. 1998. Control of translation initiation in animals. Annu. Rev. Cell Dev. Biol. 14:399-458.
19. Hodgkin, J. A., and S. Brenner. 1977. Mutations causing transformation of sexual phenotype in the nematode Caenorhabditis elegans. Genetics 86:275-287.
20. Jacobson, A., and S. W. Peltz. 1996. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem. 65:693-739.
21. Jain, R. G., L. G. Andrews, K. M. McGowan, P. H. Pekala, and J. D. Keene. 1997. Ectopic expression of Hel Nq, an RNA binding protein, increases glucose transporter (GLUT 1) expression in 3T3 L1 adipocytes. Mol. Cell. Biol. 17:954-962.
22. Jan, E., C. K. Motzny, L. E. Graves, and E. B. Goodwin. 1999. The STAR protein, GLD-1, is a translational regulator of sexual identity in Caenorhabditis elegans. EMBO J. 18:258-269.
23. Jan, E., J. W. Yoon, D. Walterhouse, P. Iannaccone, and E. B. Goodwin. 1997. Conservation of the C. elegans tra-2 3′UTR translational control. EMBO J. 16:6301-6313.
24. Jones, A. R., and T. Schedl. 1995. Mutations in gld-1, a female germ cell-specific tumor suppressor gene in Caenorhabditis elegans, affect a conserved domain also found in Src-associated protein Sam68. Genes Dev. 9:1491-1504.
25. Kozak, M. 1987. At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian cells. J. Mol. Biol. 196:947-950.
26. Kozak, M. 1989. The scanning model for translation: an update. J. Cell Biol. 108:229-241.
27. Kruys, V., O. Marinx, G. Shaw, J. Deschamps, and G. Huez. 1989. Translational blockade imposed by cytokine-derived UA-rich sequences. Science 245:852-855.
28. Kunkel, T. A. 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA 82:488-492.
29. Kuwabara, P. E., P. G. Okkema, and J. Kimble. 1992. tra-2 encodes a membrane protein and may mediate cell communication in the Caenorhabditis elegans sex determination pathway. Mol. Biol. Cell 3:461-473.
30. Legagneux, V., F. Omilli, and H. B. Osborne. 1995. Substrate-specific regulation of RNA deaderylation in Xenopus embryo and activated egg extracts. RNA 1:1001-1008.
31. Macdonald, P. M., and C. A. Smibert. 1996. Translational regulation of maternal mRNAs. Curr. Opin. Genet. Dev. 6:403-407.
32. Marinx, O., S. Bertrand, E. Karsenti, G. Huez, and V. Kruys. 1994. Fertilization of Xenopus eggs imposes a complete translational arrest of mRNAs containing 3′UUAUUUAU elements. FEBS Lett. 345:107-112.
33. McGrew, L. L., E. Dworkin-Rastl, M. B. Dworkin, and J. D. Richter. 1989. Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes Dev. 3:803-815.
34. Muckenthaler, M., N. Gunkel, R. Stripecke, and M. W. Hentze. 1997. Regulated poly(A) tail shortening in somatic cells mediated by cap-proximal translational represser proteins and ribosome association. RNA 3:983-995.
35. Murata, Y., and R. P. Wharton. 1995. Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80:747-756.
36. Newport, J., and M. Kirschner. 1982. A major developmental transition in early Xenopus embryos. I. Characterization and timing of cellular changes at the midblastula stage. Cell 30:675-686.
37. Okkema, P. G., and J. Kimble. 1991. Molecular analysis of tra-2, a sex determining gene in C. elegans. EMBO J. 10:171-176.
38. Paillard, L., V. Legagneux, and H. B. Osborne. 1996 Poly(A) metabolism in Xenopus laevis embryos: substrate-specific and default poly(A) nuclease activities are mediated by two distinct complexes. Biochimie 78:399-407.
39. Paillard, L., F. Omilli, V. Legagneux, T. Bassez, D. Maniey, and H. B. Osborne. 1998. EDEN and EDEN-BP, a cis element and an associated factor that mediate sequence-specific mRNA deadenylation in Xenopus embryos. EMBO J. 17:278-287.
40. Peng, S.-Y., C.-Y. A. Chen, N. Xu, and A.-B. Shyu. 1998. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17:3461-3470.
41. Richter, J. D. 1996. Dynamics of poly(A) addition and removal during development, p. 481-503. In J. W. B. Hershey, M. B. Mathews. and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
42. Ross, J. 1995. mRNA stability in mammalian cells. Microbiol. Rev. 59:423-450.
43. Sachs, A. B., P. Sarnow, and M. W. Hentze. 1997. Starting at the beginning, middle, and end: translation initiation in eukaryotes. Cell 89:831-838.
44. Salles, F. J., M. E. Lieberfarb, C. Wreden, J. P. Gergen, and S. Strickland. 1994. Coordinate initiation of Drosophila development by regulated polyadenylation of maternal messenger RNAs. Science 266:1996-1999.
45. Salles, F. J., and S. Stricldand. 1995. Rapid and sensitive analysis of mRNA polyadenylation states by PCR. PCR Methods Applic. 4:317-321.
46. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular chining: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
47. Sanger, F., and A. R. Coulson. 1978. The use of thin acrylamide gels for DNA sequencing. FEBS Lett. 87:107-110.
48. Schedl, T., and J. Kimble. 1988. fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 119:43-61.
49. Sheets, M. D., C. A. Fox, T. Hunt, G. Vande Woude, and M. Wickens. 1994. The 3′-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev. 8:926-938.
50. Simon, R., J. P. Tassan, and J. D. Richter. 1912. Translational control by poly(A) elongation during Xenopus development: differential repression and enhancement by a novel cytoplasmic polyadenylation element. Genes Dev. 6:2580-2591.
51. St. Johnston, D. 1995. The intracellular localization of messenger RNAs. Cell 81:161-170.
52. Tarun, S. Z., Jr., and A. B. Sachs. 1996. Association of the yeast poly(A) tail binding protein with translation initiation factor elF-4G. EMBO J. 15:7168-7177.
53. Tarun, S. Z., Jr., S. E. Wells, J. A. Deardorff, and A. B. Sachs. 1997. Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation. Proc. Natl. Acad. Sci. USA 94:9046-9051.
54. Varnum, S. M., and W. M. Wormington. 1990. Deadenylation of maternal mRNAs during Xenopus oocyte maturation does not require specific cis-sequences: a default mechanism for translational control. Genes Dev. 4:2278-2286.
55. Vernet, C., and K. Artzt. 1997. STAR, a gene family involved in signal transduction and activation of RNA. Trends Genet. 13:479-484.
56. Verrotti, A. C., S. R. Thompson, C. Wreden, S. Strickland, and M. Wickens. 1996. Evolutionary conservation of sequence elements controlling cytoplasmic polyadenylylation. Proc. Natl. Acad. Sci. USA 93:9027-9032.
57. Vize, P. D., D. A. Melton, A. Hemmati-Brivanlou, and R. M. Harland. 1991. Assays for gene function in developing Xenopus embryos. Methods Cell Biol. 36:367-387.
58. Voeltz, G. K., and J. A. Steitz. 1998. AUUUA sequences direct mRNA deadenylation uncoupled from decay during Xenopus early development. Mol. Cell. Biol. 18:7537-7545.
59. Wells, S. E., P. E. Hillner, R. D. Vale, and A. B. Sachs. 1998. Circularization of mRNA by eukaryotic translation initiation factors. Mol. Cell 2:135-140.
60. Wharton, R. P., and G. Struhl. 1991. RNA regulatory elements mediate eontrol of Drosophila body pattern by the posterior morphogen nanos. Cell 67:955-967.
61. Wickens, M., J. Kimble, and S. Strickland. 1996. Translational control of developmental decisions, p. 411-150. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y.
62. Wreden, C., A. C. Verrotti, J. A. Schisa, M. E. Lieberfarb, and S. Strickland, 1997. Nanos and pumilio establish embryonic polarity in Drosophila by promoting posterior deadenylation of hunchback mRNA. Development 124: 3015-3023.
63. Zorn, A. M., M. Grow, K. D. Patterson, T. A. Ebersole, Q. Chen, K. Artzt, and P. A. Krieg. 1997. Remarkable sequence conservation of transcripts encoding amphibian and mammalian homologues of quaking, a KH domain RNA-binding protein. Gene 188:199-206.
64. Zorn, A. M., and P. A. Krieg. 1997. The KH domain protein encoded by quaking functions as a dimer and is essential for notochord development in Xenopus embryos. Genes Dev. 11:2176-2190.